Naphthalen-1-yl Naphthalene-2-Sulfonate Enhances Arsenic Uptake and Phytoremediation Efficiency in Maize by Regulating PSII Performance and Antioxidant Responses

Year 2025, Volume: 9 Issue: 2, 386 - 399, 29.12.2025

Abidin Gümrükçüoğlu , Cansu Altuntaş

https://doi.org/10.32571/ijct.1813546

Abstract

Arsenic (As) contamination of agricultural soils threatens crop productivity and food security globally. While chelate-assisted phytoextraction enhances metal bioavailability, conventional chelating agents often exacerbate phytotoxicity and are environmentally persistent, which limits their field application. This study evaluated naphthalene-1-yl naphthalene-2-sulfonate (NNS) as a dual-mechanism agent facilitating As accumulation while mitigating toxicity in Zea mays seedlings. NNS+As treatment increased As concentration by 69% compared to As alone, while reducing lipid peroxidation and hydrogen peroxide by 37% each and moderating stress-induced proline accumulation by 37%. Antioxidant enzyme profiles were fundamentally altered: superoxide dismutase activity decreased 42% while catalase (86%), ascorbate peroxidase (25%), and guaiacol peroxidase (13%) activities increased significantly, enhancing H₂O₂ detoxification capacity. Non-enzymatic antioxidants increased substantially with NNS+As treatment: epicatechin (90%), chlorogenic acid (42%), syringic acid (42%), resveratrol (39%), and rutin (17%). Photosynthetic parameters showed remarkable recovery net photosynthetic rate, transpiration rate, and stomatal conductance increased 95-96% compared to As alone treatment, while intercellular CO₂ concentration increased 63%. Chlorophyll fluorescence analysis revealed improved photosystem II efficiency, with maximum and effective quantum yields increasing 18% and 15%, respectively, while non-photochemical quenching decreased 7-17%. These findings demonstrate NNS functions as an innovative dual-action phytoremediation enhancer, simultaneously promoting As bioaccumulation while maintaining photosynthetic functionality and cellular redox homeostasis, representing a promising environmentally sustainable alternative for integrated contaminant removal and crop protection strategies.

Keywords

Antioxidants , heavy metal , photosynthesis , maize , ROS

References

• Abbas, G., Murtaza, B., Bibi, I., Shahid, M., Niazi, N. K., Khan, M. I., Amjad, M., Hussain, M., & Natasha. (2018). Arsenic uptake, toxicity, detoxification, and speciation in plants: Physiological, biochemical, and molecular aspects. International Journal of Environmental Research and Public Health, 15(1), Article 59. https://doi.org/10.3390/ijerph15010059
• Adhikari, A., Aneefi, A. G., Sisuvanh, H., Singkham, S., Pius, M. V., Akter, F., Sohn, J. H., Kang, S. M., Kim, Y. H., & Lee, I. J. (2023). Dynamics of humic acid, silicon, and biochar under heavy metal, drought, and salinity with special reference to phytohormones, antioxidants, and melatonin synthesis in rice. International Journal of Molecular Sciences, 24(24), Article 17369. https://doi.org/10.3390/ijms242417369
• Akbulut, İ., Gürbüz, E., Rayman Ergün, A., & Baysal, T. (2021). Drying of apricots treated with Ginkgo biloba plant extract and determination of the quality properties. Journal of Advanced Research in Natural and Applied Sciences, 7(2), 145-159. https://doi.org/10.28979/jarnas.840237
• Akram, N. A., Shafiq, F., & Ashraf, M. (2017). Ascorbic acid: A potential oxidant scavenger and its role in plant development and abiotic stress tolerance. Frontiers in Plant Science, 8, Article 613. https://doi.org/10.3389/fpls.2017.00613
• Anjum, S. A., Ashraf, U., Khan, I., Tanveer, M., Khan, A. U., Shahid, M., Shakoor, A., & Wang, L. (2016). Phytohormones and plant responses to heavy metal stress: A review. Plant Growth Regulation, 80(2), 215-224. https://doi.org/10.1007/s10725-016-0174-1
• Arikan, B., Özyiğit, İ. İ., Yücel, M., Aydin, S., & Göktürk Baydar, N. (2022). Exogenous hesperidin and chlorogenic acid alleviate oxidative damage induced by arsenic toxicity in Zea mays through regulating the water status, antioxidant capacity, redox balance and fatty acid composition. Environmental Pollution, 292(Part A), Article 118389. https://doi.org/10.1016/j.envpol.2021.118389
• Arikan-Abdulveli, B. (2025). Acetylcholine treatments enhance growth, photosynthesis efficiency and stress resilience in maize seedlings exposed to arsenic. Turkish Journal of Botany, 49(1), 13-24. https://doi.org/10.55730/1300-008X.2795
• Arnon, D. I. (1950). Prof. DR Hoagland. Nature, 165(4185), 56-58. https://doi.org/10.1038/165056a0
• Atif, M., Perveen, S., Parveen, A., Mahmood, S., Saeed, M., & Zafar, S. (2022). Thiamine and indole-3-acetic acid induced modulations in physiological and biochemical characteristics of maize (Zea mays L.) under arsenic stress. Sustainability, 14(20), Article 13288. https://doi.org/10.3390/su142013288
• Bates, L. S., Waldren, R. P., & Teare, I. D. (1973). Rapid determination of free proline for water-stress studies. Plant and Soil, 39(1), 205-207. https://doi.org/10.1007/BF00018060
• Beauchamp, C., & Fridovich, I. (1971). Superoxide dismutase: Improved assays and an assay applicable to acrylamide gels. Analytical Biochemistry, 44(1), 276-287. https://doi.org/10.1016/0003-2697(71)90370-8
• Benabderrahmane, A., Atmani, M., Rhioui, W., Boutagayout, A., Errachidi, F., & Belmalha, S. (2023). Chemical and elemental composition of ammi visnaga L. And Calendula officinalis L. From meknes, Morocco. Journal of Ecological Engineering, 24(8), 84-94. https://doi.org/10.12911/22998993/165961
• Bergmeyer, H. U., & Graßl, M. (1983). Methods of enzymatic analysis (Vol. 2, 3rd ed.). Verlag Chemie.
• Chen, L., Long, C., Xu, Z., & Zhu, H. (2015). Effect of citric acid on arsenic uptake and antioxidant activity in rice seedlings under arsenic stress. Ecotoxicology and Environmental Safety, 120, 211-218. https://doi.org/10.1016/j.ecoenv.2015.06.024
• Das, S., Majumder, B., & Biswas, A. K. (2022). Comparative study on the influence of silicon and selenium to mitigate arsenic induced stress by modulating TCA cycle, GABA, and polyamine synthesis in rice seedlings. Ecotoxicology, 31(3), 468-489. https://doi.org/10.1007/s10646-022-02524-8 Evangelou, M. W. H., Ebel, M., & Schaeffer, A. (2007). Chelate assisted phytoextraction of heavy metals from soil: Effect, mechanism, toxicity, and fate of chelating agents. Chemosphere, 68(6), 989-1003. https://doi.org/10.1016/j.chemosphere.2007.01.062
• Finnegan, P. M., & Chen, W. (2012). Arsenic toxicity: The effects on plant metabolism. Frontiers in Physiology, 3, Article 182. https://doi.org/10.3389/fphys.2012.00182
• Foyer, C. H., & Noctor, G. (2011). Ascorbate and glutathione: The heart of the redox hub. Plant Physiology, 155(1), 2-18. https://doi.org/10.1104/pp.110.167569
• Fraser, C. M., & Chapple, C. (2011). The phenylpropanoid pathway in Arabidopsis. The Arabidopsis Book, 9, Article e0152. https://doi.org/10.1199/tab.0152
• Genty, B., Briantais, J. M., & Baker, N. R. (1989). The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochimica et Biophysica Acta (BBA)- Bioenergetics, 990(1), 87-92. https://doi.org/10.1016/S0304-4165(89)80016-9
• Gill, S. S., & Tuteja, N. (2010). Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiology and Biochemistry, 48(12), 909-930. https://doi.org/10.1016/j.plaphy.2010.08.016
• Gururani, M. A., Venkatesh, J., & Tran, L. S. P. (2015). Regulation of photosynthesis during abiotic stress-induced photoinhibition. Molecular Plant, 8(9), 1304-1320. https://doi.org/10.1016/j.molp.2015.05.005
• Hasanuzzaman, M., Bhuyan, M. H. M. B., Zulfiqar, F., Raza, A., Mohsin, S. M., Al Mahmud, J., Fujita, M., & Fotopoulos, V. (2020). Reactive oxygen species and antioxidant defense in plants under abiotic stress: Revisiting the crucial role of enzymatic and nonenzymatic antioxidants. Antioxidants, 9(8), Article 681. https://doi.org/10.3390/antiox9080681
• Hasanuzzaman, M., Hossain, M. A., da Silva, J. A. T., & Fujita, M. (2011). Plant response and tolerance to abiotic oxidative stress: Antioxidant defense is a key factor. In A. K. Shanker & B. Venkateswarlu (Eds.), Crop stress and its management: Perspectives and strategies (pp. 261-315). Springer Netherlands.
• Heath, R. L., & Packer, L. (1968). Photoperoxidation in isolated chloroplasts: I. Kinetics and stoichiometry of fatty acid peroxidation. Archives of Biochemistry and Biophysics, 125(1), 189-198. https://doi.org/10.1016/0003-9861(68)90654-1
• Kamal, M. A., Iqbal, M., Saleem, M. H., Imran, M., Ahmad, S., Hussain, S., Fahad, S., & Cheema, M. (2023). Effect of different levels of EDTA on phytoextraction of heavy metals and associated oxidative responses. Frontiers in Microbiology, 14, Article 1228117. https://doi.org/10.3389/fmicb.2023.1228117
• Krause, G. H., & Weis, E. (1991). Chlorophyll fluorescence and photosynthesis: The basics. Annual Review of Plant Physiology and Plant Molecular Biology, 42, 313-349. https://doi.org/10.1146/annurev.pp.42.060191.001525
• Lim, T. T., Chui, P. C., & Goh, K. H. (2005). Process evaluation for optimization of EDTA use and recovery for heavy metal removal from a contaminated soil. Chemosphere, 58(8), 1031-1040. https://doi.org/10.1016/j.chemosphere.2004.09.046
• Liu, J., Osbourn, A., & Ma, P. (2015). MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Molecular Plant, 8(5), 689-708. https://doi.org/10.1016/j.molp.2015.03.012
• Liu, C.P., Luo, C.L., Gao, Y., Li, F.B., Lin, L.W., Wu, C.A., Li, X.D., 2010. Arsenic contamination and potential health risk implications at an abandoned tungsten mine, southern China. Environ. Pollut. 158, 820-826. https://doi.org/10.1016/j.envpol.2009.09.029
• Ma, L. Q., Komar, K. M., Tu, C., Zhang, W., Cai, Y., & Kennelley, E. D. (2001). A fern that hyperaccumulates arsenic. Nature, 409(6820), 579. https://doi.org/10.1038/35054664
• Malik, J. A., Goel, S., Kaur, N., Sharma, S., Singh, I., & Nayyar, H. (2012). Selenium antagonises the toxic effects of arsenic on mungbean (Phaseolus aureus Roxb.) plants by restricting its uptake and enhancing the antioxidative and detoxification mechanisms. Environmental and Experimental Botany, 77, 242-248. https://doi.org/10.1016/j.envexpbot.2011.12.001
• Mansoor, S., Ali, A., Kour, N., Bornhorst, J., AlHarbi, K., Rinklebe, J., Abd El Moneim, D., Ahmad, P., & Chung, Y. S. (2023). Heavy metal induced oxidative stress mitigation and ROS scavenging in plants. Plants, 12(16), Article 3003. https://doi.org/10.3390/plants12163003
• Michalak, A. (2006). Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies, 15(4), 523-530.
• Mittler, R. (2002). Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7(9), 405-410. https://doi.org/10.1016/S1360-1385(02)02312-9
• Mousavi, S. R., Niknejad, Y., Fallah, H., & Tari, D. B. (2020). Methyl jasmonate alleviates arsenic toxicity in rice. Plant Cell Reports, 39(8), 1041-1060. https://doi.org/10.1007/s00299-020-02547-7
• Mylona, P. V., Polidoros, A. N., & Scandalios, J. G. (1998). Modulation of antioxidant responses by arsenic in maize. Free Radical Biology and Medicine, 25(4-5), 576-585. https://doi.org/10.1016/S0891-5849(98)00090-2
• Nakano, Y., & Asada, K. (1987). Purification of ascorbate peroxidase in spinach chloroplasts; Its inactivation in ascorbate-depleted medium and reactivation by monodehydroascorbate radical. Plant and Cell Physiology, 28(1), 131-140. https://doi.org/10.1093/oxfordjournals.pcp.a077268
• Nar, H., Saglam, A., Terzi, R., Várkonyi, Z., & Kadioglu, A. (2009). Leaf rolling and photosystem II efficiency in Ctenanthe setosa exposed to drought stress. Photosynthetica, 47(3), 429-436. https://doi.org/10.1007/s11099-009-0066-8
• Naujokas, M. F., Anderson, B., Ahsan, H., Aposhian, H. V., Graziano, J. H., Thompson, C., & Suk, W. A. (2013). The broad scope of health effects from chronic arsenic exposure: Update on a worldwide public health problem. Environmental Health Perspectives, 121(3), 295-302. https://doi.org/10.1289/ehp.1205875
• Rahman, M. M., Das, A. K., Sultana, S., Ghosh, P. K., Islam, M. R., Keya, S. S., Ahmed, M., & Mostofa, M. G. (2023). Biochar potentially enhances maize tolerance to arsenic toxicity by improving physiological and biochemical responses to excessive arsenate. Biochar, 5(1), Article 71. https://doi.org/10.1007/s42773-023-00270-6
• Römkens, P., Bouwman, L., Japenga, J., & Draaisma, C. (2002). Potentials and drawbacks of chelate-enhanced phytoremediation of soils. Environmental Pollution, 116(1), 109-121. https://doi.org/10.1016/S0269-7491(01)00150-6
• Rudrapal, M., Khairnar, S. J., Khan, J., Dukhyil, A. B., Ansari, M. A., Alomary, M. N., Alshabrmi, F. M., Palai, S., Deb, P. K., & Devi, R. (2022). Dietary polyphenols and their role in oxidative stress-induced human diseases: Insights into protective effects, antioxidant potentials and mechanism(s) of action. Frontiers in Pharmacology, 13, Article 806470. https://doi.org/10.3389/fphar.2022.806470
• Saleem, M. H., Rehman, M., Kamran, M., Afzal, J., Xiang, W., & Liu, L. (2020). Ethylenediaminetetraacetic Acid (EDTA) mitigates the toxic effect of excessive copper concentrations on growth, gaseous exchange and chloroplast ultrastructure of Corchorus capsularis L. Plants, 9(6), Article 756. https://doi.org/10.3390/plants9060756
• Sattar, A., Sher, A., Abourehab, M. A. S., Ijaz, M., Nawaz, M., Ul-Allah, S., Abbas, T., Shah, A. N., Imam, M. U., Abdelsalam, N. R., Hasan, M. E., & Javaid, M. M. (2022). Application of silicon and biochar alleviates the adversities of arsenic stress in maize by triggering the morpho-physiological and antioxidant defense mechanisms. Frontiers in Environmental Science, 10, Article 979049. https://doi.org/10.3389/fenvs.2022.979049
• Shaghaleh, H., Alhaj Hamoud, Y., Saleem, M. H., Mansoor, S., Ali, S., Abbas, S., Sheteiwy, M. S., Zhou, G., & Hamoud, Y. A. (2025). Phytohormonal modulation alleviates arsenic toxicity in rice by enhancing antioxidant defenses, proline metabolism, and arsenic detoxification mechanisms. Scientific Reports, 15(1), Article 26953. https://doi.org/10.1038/s41598-025-11629-z Shahid, M., Austruy, A., Echevarria, G., Arshad, M., Sanaullah, M., Aslam, M., Nadeem, M., Nasim, W., & Dumat, C. (2014). EDTA-enhanced phytoremediation of heavy metals: A review. Soil and Sediment Contamination: An International Journal, 23(4), 389-416. https://doi.org/10.1080/15320383.2014.831029
• Shankar, S., Shanker, U., & Shikha. (2014). Arsenic contamination of groundwater: A review of sources, prevalence, health risks, and strategies for mitigation. The Scientific World Journal, 2014, Article 304524. https://doi.org/10.1155/2014/304524
• Sharma, I. (2012). Arsenic induced oxidative stress in plants. Biologia, 67(3), 447-453. https://doi.org/10.2478/s11756-012-0024-y
• Shinta, Y. C., Zaman, B., & Sumiyati, S. (2021). Citric acid and EDTA as chelating agents in phytoremediation of heavy metal in polluted soil: A review. IOP Conference Series: Earth and Environmental Science, 896(1), Article 012023. https://doi.org/10.1088/1755-1315/896/1/012023
• Shri, M., Dubey, S., Dwivedi, S., Singh, P. K., & Tripathi, R. D. (2024). Long-distance translocation mechanism of arsenic from soil to rice grain. In Arsenic in rice (pp. 75-94). Apple Academic Press.
• Singh, S., Parihar, P., Singh, R., Singh, V. P., & Prasad, S. M. (2015). Heavy metal tolerance in plants: Role of transcriptomics, proteomics, metabolomics, and ionomics. Frontiers in Plant Science, 6, Article 1143. https://doi.org/10.3389/fpls.2015.01143
• Smirnoff, N. (2000). Ascorbic acid: Metabolism and functions of a multi-facetted molecule. Current Opinion in Plant Biology, 3(3), 229-235. https://doi.org/10.1016/S1369-5266(00)80070-9
• Smith, A. H., Lingas, E. O., & Rahman, M. (2000). Contamination of drinking-water by arsenic in Bangladesh: A public health emergency. Bulletin of the World Health Organization, 78(9), 1093-1103.
• Stoeva, N., & Bineva, T. (2003). Oxidative changes and photosynthesis in oat plants grown in As-contaminated soil. Bulgarian Journal of Plant Physiology, 29(1-2), 87-95.
• Tahjib-Ul-Arif, M., Zahan, M. I., Karim, M. M., Imran, S., Hunter, C. T., Islam, M. S., Mia, M. A. B., Hannan, M. A., Rhaman, M. S., Hossain, M. A., Brestic, M., Skalicky, M., & Murata, Y. (2021). Citric acid-mediated abiotic stress tolerance in plants. International Journal of Molecular Sciences, 22(13), Article 7235. https://doi.org/10.3390/ijms22137235
• Tamma, A. A., Ali, S., & Wang, H. (2025). Advancing phytoremediation: A review of soil amendments. Sustainability, 17(13), Article 5688. https://doi.org/10.3390/su17135688
• Tchounwou, P. B., Yedjou, C. G., Patlolla, A. K., & Sutton, D. J. (2012). Heavy metal toxicity and the environment. In Molecular, clinical and environmental toxicology: Volume 3: Environmental toxicology (pp. 133–164). Springer.
• Urbanek, H., Kuźniak-Gębarowska, E., & Herka, K. (1991). Elicitation of defense responses in bean leaves by Botrytis cinerea polygalacturonase. Acta Physiologiae Plantarum, 13, 43–50.
• Vamerali, T., Bandiera, M., & Mosca, G. (2010). Field crops for phytoremediation of metal-contaminated land: A review. Environmental Chemistry Letters, 8(1), 1–17. https://doi.org/10.1007/s10311-009-0268-0
• Van Kooten, O., & Snel, J. F. H. (1990). The use of chlorophyll fluorescence nomenclature in plant stress physiology. Photosynthesis Research, 25, 147–150. https://doi.org/10.1007/BF00033156
• Velikova, V., Yordanov, I., & Edreva, A. (2000). Oxidative stress and some antioxidant systems in acid-rain-treated bean plants: Protective role of exogenous polyamines. Plant Science, 151, 59–66. https://doi.org/10.1016/S0168-9452(99)00197-1
• Vogt, T. (2010). Phenylpropanoid biosynthesis. Molecular Plant, 3, 2–20. https://doi.org/10.1093/mp/ssp106
• World Health Organization. (2022). Arsenic – Fact sheet. WHO Press. Xu, W., Dubos, C., & Lepiniec, L. (2015). Transcriptional control of flavonoid biosynthesis by MYB–bHLH–WD40 complexes. Trends in Plant Science, 20, 176–185. https://doi.org/10.1016/j.tplants.2014.12.001
• Yan, A., Wang, Y., Tan, S. N., Mohd Yusof, M. L., Ghosh, S., & Chen, Z. (2020). Phytoremediation: A promising approach for revegetation and pollution mitigation. Frontiers in Plant Science, 11, 359. https://doi.org/10.3389/fpls.2020.00359
• Yetişsin, F., & Korkmaz, A. (2023). Synthesis and characterization of naphthalene-sulfonate hybrid structures and their effects on abiotic stress indicators in maize. Anadolu Orman Araştırmaları Dergisi, 9, 89–95. https://doi.org/10.53516/ajfr.1257960
• Zhao, F. J., Ma, J. F., Meharg, A. A., & McGrath, S. P. (2009). Arsenic uptake and metabolism in plants. New Phytologist, 226(1), 148–162. https://doi.org/10.1111/j.1469-8137.2008.02716.x
• Zhao, F. J., McGrath, S. P., & Meharg, A. A. (2010). Arsenic as a food chain contaminant: Mechanisms of plant uptake and metabolism and mitigation strategies. Annual Review of Plant Biology, 61, 535–559. https://doi.org/10.1146/annurev-arplant-042809-112152